Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions

Abstract

Disease resistance of plants involves two distinct forms of chemical communication with the pathogen: recognition and defense. Both are essential components of a highly complex, multifaceted defense response, which begins with non-self recognition through the perception of pathogen-derived signal molecules and results in the production, inter alia, of antibiotically active compounds (phytoalexins) and cell wall-reinforcing material around the infection site. To elucidate the molecular details and the genomic basis of the underlying chains of events, we used two different experimental systems: suspension-cultured cells of Petroselinum crispum (parsley) and wildtype as well as mutant plants of Arabidopsis thaliana. Particular emphasis was placed on the structural and functional identification of signal and defense molecules, and on the mechanisms of signal perception, intracellular signal transduction and transcriptional reprogramming, including the structural and functional characterization of the responsible cis-acting gene promoter elements and transacting regulatory proteins. Comparing P. crispum and A. thaliana allows us to distinguish species-specific defense mechanisms from more universal responses, and furthermore provides general insights into the nature of the interactions. Despite the complexity of the pathogen defense response, it is experimentally tractable, and knowledge gained so far has opened up a new realm of gene technologyassisted strategies for resistance breeding of crop plants. Most plant͞pathogen interactions are fierce battles of attack and counterattack. These battles are fought with highly sophisticated means for the survival of the individual and, in the end, of the entire population or species. On the plant side, the most immediate defense response includes the reprogramming of cellular metabolism and highly dynamic, structural rearrangements within and around the attacked cells. In the cases of locally invading, fungal or fungus-like pathogens, the counterstroke of the plant commences in a highly localized fashion with the perception of chemical and physical signals from the intruder and ends with the accumulation of soluble, antibiotically active compounds and wall-bound, barrier-forming substances. The initiating event, attempted penetration of a potential pathogen, immediately activates an elaborate safe-guard system of non-self recognition based on specifically adapted plant receptors. These receptors recognize characteristic pathogen-borne surface molecules and transduce that information to numerous genes through a network of intracellular signaling cascades that orchestrate an extensive, defense-oriented transcriptional reprogramming of the affected cell. Among the major changes in cellular metabolism is the rapid accumulation of various secondary metabolites, some of which are likely to be integral to the complex, multicomponent defense response.This network of events, from the initial stage of recognition by the plant to the successful confinement or death of the pathogen, is ...

Universally occurring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves

“…Nevertheless, our present data on A. thaliana, as well as those (Fig. 5) extending earlier studies on cultured P. crispum cells (Kauss et al, 1993;Franke et al, 1998), are in full accord with, and further confirm, the general conclusion (Hahlbrock et al, 2003) that the three analogous series of 4-hydroxy-, 4-hydroxy-3-methoxy-, and 4-hydroxy-3,5-dimethoxybenzaldehyde, -benzoate and -cinnamate together constitute a characteristic set of universally occurring, aromatic cell wall-bound compounds in higher plants.…”

“…Large changes in secondary metabolism, including the accumulation of phytoalexins and aromatic cell wallbound compounds, are among the earliest detectable results of the extensive transcriptional reprogramming that occurs in challenged plant cells during plant/ pathogen interactions (Somssich and Hahlbrock, 1998;Dixon, 2001;Hahlbrock et al, 2003). Using soluble extracts from Arabidopsis thaliana leaves, we have previously shown that, in addition to the characteristic phytoalexin of this species, camalexin, several other indolic metabolites were strongly and rapidly induced upon infection.…”

The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes

“…The less frequently occurring box A (28) is not present in any one of the four At4CL gene promoters without at least one (At4CL3) or two (At4CL4) mismatches. An absolute singularity among all known 4CL genes is the occurrence of three perfect TATA-proximal W-box sequences (25) in the At4CL4 gene promoter, two of which have recently been shown to fulfil the operational W-box criterion of WRKY transcription factor binding (14).…”

“…This latter discovery, in the context of our long-term interest in understanding the functional diversity of phenylpropanoid metabolism in conjunction with its genetic background in A. thaliana (14), prompted us to further characterize this rare sinapate-activating At4CL and define its position within the At4CL gene family. Here, we verify its identity as a previously undetected fourth isoenzyme (At4CL4) in A. thaliana, compare its structural and putative functional characteristics with those of the other three family members, propose a sequence for the stepwise evolution of the four At4CLs as a basis for the diversification of phenylpropanoid metabolism, and discuss the results in relation to the substructure of the overall plant 4CL superfamily.…”

An integrative statistical method to explore herbivory-specific responses in plants

“…[1][2][3][4] Experiments designed to study such intricate networks often have a complex factorial structure, obtained by assessing plant responses in different conditions/treatments, tissue types or genetic contexts. Among the major problems associated with the statistical analysis of multifactorial experimental designs are those of gene prioritization and of large numbers of false positives.…”